Parasites that change predator or prey behaviour can have keystone effects on community composition

Parasites play pivotal roles in structuring communities, often via indirect interactions with non-host species. These effects can be density-mediated (through mortality) or trait-mediated (behavioural, physiological and developmental), and may be crucial to population interactions, including biological invasions. For instance, parasitism can alter intraguild predation (IGP) between native and invasive crustaceans, reversing invasion outcomes. Here, we use mathematical models to examine how parasite-induced trait changes influence the population dynamics of hosts that interact via IGP. We show that trait-mediated indirect interactions impart keystone effects, promoting or inhibiting host coexistence. Parasites can thus have strong ecological impacts, even if they have negligible virulence, underscoring the need to consider trait-mediated effects when predicting effects of parasites on community structure in general and biological invasions in particular.     

A keystone effect for parasites in intraguild predation?

Intraguild predation (IGP) is common in communities, yet theory suggests it should not often persist and coexistence of participating species should be rare. As parasitism can play keystone roles in interactions between competitors, and between predators and prey, here we examine the role of parasites in maintaining IGP. We used numerical exploration of population dynamic equations to determine coexistence and exclusion zones for two species engaged in IGP with shared parasitism. We demonstrate that parasitism increases the range of conditions leading to coexistence when the parasite exerts a greater deleterious effect on the 'stronger' species in terms of the combined effects of competition and predation. Such a parasite can enable an inferior competitor that is also the less predatory to persist, and may actually lead to numerical dominance of this species.     

Resetting our expectations for parasites and their effects on species interactions: a meta-analysis

Despite the ubiquitous nature of parasitism, how parasitism alters the outcome of host–species interactions such as competition, mutualism and predation remains unknown. Using a phylogenetically informed meta-analysis of 154 studies, we examined how the mean and variance in the outcomes of species interactions differed between parasitized and non-parasitized hosts. Overall, parasitism did not significantly affect the mean or variance of host–species interaction outcomes, nor did the shared evolutionary histories of hosts and parasites have an effect. Instead, there was considerable variation in outcomes, ranging from strongly detrimental to strongly beneficial for infected hosts. Trophically-transmitted parasites increased the negative effects of predation, parasites increased and decreased the negative effects of interspecific competition for parasitized and non-parasitized heterospecifics, respectively, and parasites had particularly strong negative effects on host species interactions in freshwater and marine habitats, yet were beneficial in terrestrial environments. Our results illuminate the diverse ways in which parasites modify critical linkages in ecological networks, implying that whether the cumulative effects of parasitism are considered detrimental depends not only on the interactions between hosts and their parasites but also on the many other interactions that hosts experience.     

An acanthocephalan parasite mediates intraguild predation between invasive and native freshwater amphipods (Crustacea)

1. The balance of predation between closely related invasive and native species can be an important determinant of the success or failure of biological invasions. In Irish freshwaters, the introduced amphipod Gammarus pulex has replaced the native G. duebeni celticus, possibly through differential mutual intraguild predation (IGP). Theoretically, parasitism could mediate such predation and hence the invasion outcome. However, this idea remains poorly studied. 2. In a field survey, we show that the acanthocephalan parasite Echinorynchus truttae is present in more G. pulex populations than G. d. celticus populations. In addition, within parasitised populations, E. truttae is more prevalent in the invader than in the native. 3. We show for the first time that an acanthocephalan parasite mediates predation between its intermediate macroinvertebrate hosts. In a field experiment, E. truttae parasitism of the invader lowered IGP upon the unparasitised native. In laboratory experiments, parasitism of G. pulex significantly reduced their predatory impact on recently moulted female G. d. celticus. Parasitism also appeared to cause reduction in predatory behaviour, such as attacks per contact on precopula guarded female natives. 4. We conclude that higher parasite prevalence in invaders as compared with natives, by mediation of interspecific interactions, could promote species coexistence, or at least slow species replacements, in this particular biological invasion.     

Prey, predators, parasites: intraguild predation or simpler community modules in disguise?

1.?Competition and predation are at the heart of community ecology. The theoretical concept of intraguild predation (IGP) combines these key interactions in a single community module. Because IGP is believed to be ubiquitous in nature, it has been subject to extensive research, and there exists a well-developed theoretical framework. 2.?We show that a general class of IGP models can be transformed to simpler, but equivalent community structures. This rather unexpected simplification depends critically on the property of 'indiscriminate predation', which we define broadly as the top-predator not distinguishing between its two different prey species. 3.?In a broader context, the great importance of IGP and of the simplifying transformation we report here is enhanced by the recent insight that the basic IGP structure extends naturally to host-parasitoid and host-pathogen communities. We show that parasites infecting prey (predators) tend to render IGP effectively into exploitative competition (tritrophic food chain, respectively). 4.?The equivalence between the original and simplified community module makes it possible to take advantage from already existing insights. We illustrate this by means of an eco-epidemiological IGP model that is strikingly similar to a classical exploitative competition model. 5.?The change of perspective on certain community modules may contribute to a better understanding of food web dynamics. In particular, it may help explain the interactions in food webs that include parasites. Given the ubiquity of parasitism, food webs may appear in a different light when they are transformed to their simplified analogue.     

Quantifying the relative importance of variation in predation and the environment for species coexistence

Coexistence and food web theory are two cornerstones of the long‐standing effort to understand how species coexist. Although competition and predation are known to act simultaneously in communities, theory and empirical study of these processes continue to be developed largely independently. Here, we integrate modern coexistence theory and food web theory to simultaneously quantify the relative importance of predation and environmental fluctuations for species coexistence. We first examine coexistence in a theoretical, multitrophic model, adding complexity to the food web using machine learning approaches. We then apply our framework to a stochastic model of the rocky intertidal food web, partitioning empirical coexistence dynamics. We find the main effects of both environmental fluctuations and variation in predator abundances contribute substantially to species coexistence. Unexpectedly, their interaction tends to destabilise coexistence, leading to new insights about the role of bottom‐up vs. top‐down forces in both theory and the rocky intertidal ecosystem.     

Roles of parasites in animal invasions

Biological invasions are global threats to biodiversity and parasites might play a role in determining invasion outcomes. Transmission of parasites from invading to native species can occur, aiding the invasion process, whilst the 'release' of invaders from parasites can also facilitate invasions. Parasites might also have indirect effects on the outcomes of invasions by mediating a range of competitive and predatory interactions among native and invading species. Although pathogen outbreaks can cause catastrophic species loss with knock-on effects for community structure, it is less clear what impact persistent, sub-lethal parasitism has on native-invader interactions and community structure. Here, we show that the influence of parasitism on the outcomes of animal invasions is more subtle and wide ranging than has been previously realized.     

Effects of productivity, disturbance, and ecosystem size on food-chain length: insights from a metacommunity model of intraguild predation

Traditionally, productivity and disturbance have been hypothesized as important determinants of food-chain length. More recently, growing empirical evidence suggests a strong role of ecosystem size. To theoretically explore the effects of basal productivity, disturbance, and ecosystem size on food-chain length, we develop and analyze a metacommunity model of intraguild predation (IGP). The model finds that, when local IGP is weak, increasing basal productivity, weakening disturbance, and increasing ecosystem size will generally increase food-chain length. When local IGP is strong, by contrast, increasing basal productivity or weakening disturbance favors intraguild predators and hinders the coexistence of intraguild predators and intraguild prey, limiting food-chain length. In contrast, increasing ecosystem size can promote coexistence even when local IGP is strong, increasing food-chain length through inserting intraguild prey and changing the degree of omnivory by intraguild predators. Intraguild prey needs to be the superior colonizer to intraguild predators for this to occur. We discuss that these theoretical predictions appear consistent with empirical patterns.     

Impacts of enemy-mediated effects and the additivity of interactions in an insect trophic system

In this study, we used data from both experiments and mathematical simulations to analyze the consequences of the interacting effects of intraguild predation (IGP), cannibalism and parasitism occurring in isolation and simultaneously in trophic interactions involving two blowfly species under shared parasitism. We conducted experiments to determine the short-term response of two blowfly species to these interactions with respect to their persistence. A mathematical model was employed to extend the results obtained from these experiments to the long-term consequences of these interactions for the persistence of the blowfly species. Our experimental results revealed that IGP attenuated the strength of the effects of cannibalism and parasitism between blowfly host species, increasing the probability of persistence of both populations. The simulations obtained from the mathematical model indicated that IGP is a key interaction for the long-term dynamics of this system. The presence of different species interacting in a tri-trophic system relaxed the severity of the effects of a particular interaction between two species, changing species abundances and promoting persistence through time. This pattern was related to indirect interactions with a third species, the parasitoid species included in this study.     

Emerging niche clustering results from both competition and predation

Understanding species coexistence has been a central question in ecology for decades, and the notion that competing species need to differ in their ecological niche for stable coexistence has dominated. Recent theoretical and empirical work suggests differently. Species can also escape competitive exclusion by being similar, leading to clusters of species with similar traits. This theory has so far only been explored under competition. By combining mathematical and numerical analyses, we reveal that competition and predation are equally capable to promote clusters of similar species in prey–predator communities, their relative importance being modulated by resource availability. We further show that predation has a stabilizing effect on clustering patterns, making the clusters more diverse. Our results merge different ecological theories and bring new light to the emergent neutrality theory by adding the perspective of trophic interactions. These results open new perspectives to the study of trait distributions in ecological interaction networks.     

Examining the relative importance of spatial and nonspatial coexistence mechanisms

Much of the work on species coexistence has focused on the presence or absence of single mechanisms. Most theoretical frameworks, however, do not allow one to measure the strength of coexistence mechanisms, and so it has been difficult to determine the relative importance of each mechanism when multiple mechanisms are present. We present a model inspired by the California red scale system, in which two parasitoids coexist on a single, tree-dwelling host-scale insect. Previous work suggests that coexistence may be promoted both by intraguild predation (IGP) and by differing preferences for hosts on stems versus hosts on leaves (habitat preference). By applying an analytic framework that quantifies the strengths of spatial coexistence mechanisms, we are able to measure the individual contributions of IGP, habitat preference, and their interaction to maintaining coexistence. We find that habitat preference is much more effective at promoting coexistence in this model than in IGP. Furthermore, the effects of habitat preference and IGP are not independent. When the two parasitoids prefer different habitats, the coexistence-promoting effects of habitat preference are strengthened by IGP if IGP gives a moderate advantage to the inferior competitor. If IGP either confers an excessive advantage or favors the superior competitor, it can diminish the coexistence region.     

Biotic indirect effects: a neglected concept in invasion biology

Indirect effects involve more than two species and are defined as how one species alters the effect that another species has on a third. These complex interactions are often overlooked in studies of interactions between alien and native species, and their role in influencing biological invasions has been rarely considered. Based on a comprehensive review of the invasion biology literature, we examine the evidence for the occurrence of four of the most commonly documented indirect effects (apparent competition, indirect mutualism/commensalism, exploitative competition, and trophic cascades) in the invasion process. Studies investigating indirect effects in the context of invasion biology are relatively rare, but have been increasing in recent years, and there are sufficient examples to indicate that this kind of interaction is likely to be more common than is currently recognized. Whether indirect interactions are mediated by an alien or a native species, and whether they occur between ecologically similar or dissimilar alien and native species, depends in part on the type of interaction considered and no predictable patterns were detected in the literature. Further empirical studies will help to elucidate such patterns. At this stage, the inherent unpredictability of indirect interactions means that their impacts in relation to invasions are particularly challenging for land managers to deal with, and their role in invasions is a complex, but is a valuable area of investigation for researchers.     

Trophic supplements to intraguild predation

Intraguild predation (IGP) is a dominant community module in terrestrial food webs that occurs when multiple consumers feed both on each other and on a shared prey. This specific form of omnivory is common in terrestrial communities and is of particular interest for conservation biology and biological control given its potential to disrupt management of threatened or pest species. Extensive theory exists to describe the dynamics of three-species IGP, but these models have largely overlooked the potential for other, exterior interactions, to alter the dynamics within the IGP module. We investigated how three forms of feeding outside of the IGP module by intraguild predators (i.e. trophic supplementation) affect the dynamics of the predators (both IG predator and IG prey) and their shared resource. Specifically, we examined how the provision of a constant donor-controlled resource, the availability of an alternative prey species, and predator plant-feeding affect the dynamics of IGP models. All three forms of trophic supplements modified the basic expectations of IGP theory in two important ways, and their effects were similar. First, coexistence was possible without the IG prey being a superior competitor for the original shared resource if the IG prey could effectively exploit one of the types of trophic supplements. However, supplements to the IG predator restricted the potential for coexistence. Second, supplements to the IG prey ameliorated the disruptive effects of the IG predator on the suppression of the shared resource, promoting effective control of the resource in the presence of both predators. Consideration of these three forms of trophic supplementation, all well documented in natural communities, adds substantial realism and predictive power to intraguild predation theory.     

Interference interactions, co-existence and conservation of mammalian carnivores

Abstract.  The shift in emphasis from single species to ecosystem conservation is revealing how community interactions can potentially influence single species viability and conservation. Although there is much theory and empirical data concerning the dynamic consequences of exploitative interactions, there is still a very poor understanding of the effects of interference interactions. Recent studies, as shown in this review, have documented widespread effects of such interactions among mammalian carnivores. Harassment, loss of kills and intraguild predation have been documented in a wide range of species. The demonstrated effects also include avoidance of larger carnivores in both time and space and reductions in one species density or even total exclusion from certain habitats or regions. Our review of the literature thus provides a range of empirical examples that together demonstrate that these interactions have very important implications on carnivore demography. We believe that the effects of interference might differ strongly from the effects of exploitative competition. This is because interference might have the potential to affect population growth in an inverse density-dependent manner and thereby also reduce population growth at low densities, therefore increasing extinction probabilities. These factors need to be considered when planning future multi-species conservation. Further research into the temporal and spatial aspects of co-existence are required if diverse guilds and communities are to be conserved.     

Modelling parasitism and predation of mosquitoes by water mites

Parasitism and predation are two ecological interactions that can occur simultaneously between two species. This is the case of Culicidae (Insecta: Diptera) and water mites (Acari: Hydrachnidia). The larva mites are~parasites of aquatic and semiaquatic insects, and deutonymphs and adults are predators of insect larvae and eggs. Since several families of water mites are associated with mosquitoes there is an interest in the potential use of these mites as biological control agents. The aim of this paper is to use mathematical modelling and analysis to assess the impact of predation and parasitism in the mosquito population. We propose a system of ordinary differential equations to model the interactions among the larval and adult stages of mosquitoes and water mites. The model exhibits three equilibria: the first equilibrium point corresponds to the state where the two species are absent, the second one to the state where only mosquitoes are present (water mites need insects to complete their life cycle), and the third one is the coexistence equilibrium. We analyze conditions for the asymptotic stability of equilibria, supported by analytical and numerical methods. We discuss the different scenarios that appear when we change the parasitism and predation parameters. High rates of parasitism and moderate predation can drive two species to a stable coexistence.     

The enemy of my enemy is my friend: intraguild predation between invaders and natives facilitates coexistence with shared invasive prey

Understanding and predicting the outcomes of biological invasions is challenging where multiple invader and native species interact. We hypothesize that antagonistic interactions between invaders and natives could divert their impact on subsequent invasive species, thus facilitating coexistence. From field data, we found that, when existing together in freshwater sites, the native amphipod Gammarus duebeni celticus and a previous invader G. pulex appear to facilitate the establishment of a second invader, their shared prey Crangonyx pseudogracilis. Indeed, the latter species was rarely found at sites where each Gammarus species was present on its own. Experiments indicated that this may be the result of G. d. celticus and G. pulex engaging in more intraguild predation (IGP) than cannibalism; when the ‘enemy’ of either Gammarus species was present, that is, the other Gammarus species, C. pseudogracilis significantly more often escaped predation. Thus, the presence of mutual enemies and the stronger inter- than intraspecific interactions they engage in can facilitate other invaders. With some invasive species such as C. pseudogracilis having no known detrimental effects on native species, and indeed having some positive ecological effects, we also conclude that some invasions could promote biodiversity and ecosystem functioning.     

The influence of interspecific interactions on species range expansion rates

Ongoing and predicted global change makes understanding and predicting species' range shifts an urgent scientific priority. Here, we provide a synthetic perspective on the so far poorly understood effects of interspecific interactions on range expansion rates. We present theoretical foundations for how interspecific interactions may modulate range expansion rates, consider examples from empirical studies of biological invasions and natural range expansions as well as process‐based simulations, and discuss how interspecific interactions can be more broadly represented in process‐based, spatiotemporally explicit range forecasts. Theory tells us that interspecific interactions affect expansion rates via alteration of local population growth rates and spatial displacement rates, but also via effects on other demographic parameters. The best empirical evidence for interspecific effects on expansion rates comes from studies of biological invasions. Notably, invasion studies indicate that competitive dominance and release from specialized enemies can enhance expansion rates. Studies of natural range expansions especially point to the potential for competition from resident species to reduce expansion rates. Overall, it is clear that interspecific interactions may have important consequences for range dynamics, but also that their effects have received too little attention to robustly generalize on their importance. We then discuss how interspecific interactions effects can be more widely incorporated in dynamic modeling of range expansions. Importantly, models must describe spatiotemporal variation in both local population dynamics and dispersal. Finally, we derive the following guidelines for when it is particularly important to explicitly represent interspecific interactions in dynamic range expansion forecasts: if most interacting species show correlated spatial or temporal trends in their effects on the target species, if the number of interacting species is low, and if the abundance of one or more strongly interacting species is not closely linked to the abundance of the target species.     

Niche theory for within-host parasite dynamics: Analogies to food web modules via feedback loops

Why do parasites exhibit a wide dynamical range within their hosts? For instance, why does infecting dose either lead to infection or immune clearance? Why do some parasites exhibit boom-bust, oscillatory dynamics? What maintains parasite diversity, that is coinfection v single infection due to exclusion or priority effects? For insights on parasite dose, dynamics and diversity governing within-host infection, we turn to niche models. An omnivory food web model (IGP) blueprints one parasite competing with immune cells for host energy (PIE). Similarly, a competition model (keystone predation, KP) mirrors a new coinfection model (2PIE). We then drew analogies between models using feedback loops. The following three points arise: first, like in IGP, parasites oscillate when longer loops through parasites, immune cells and resource regulate parasite growth. Shorter, self-limitation loops (involving resources and enemies) stabilise those oscillations. Second, IGP can produce priority effects that resemble immune clearance. But, despite comparable loop structure, PIE cannot due to constraints imposed by production of immune cells. Third, despite somewhat different loop structure, KP and 2PIE share apparent and resource competition mechanisms that produce coexistence (coinfection) or priority effects of prey or parasites. Together, this mechanistic niche framework for within-host dynamics offers new perspective to improve individual health.     

Intraguild predation in biological control: consideration of multiple resource species

Theoretical models of intraguild predation (IGP) predict that IGP decreases the effectiveness of biological control while many empirical studies do not agree with this prediction. In this study, I discuss the importance of explicit consideration of multiple resource species that has been neglected in most theoretical IGP models. In the previous models of IGP, a single resource species represented the pest species. However, there are multiple resource species (e.g., multiple pest species or aggregates of pest and non-pest species) in real systems. This study shows that models with multiple resource species can predict a variety of outcomes including those consistent with the empirical observations. The explicit consideration of resource species is useful for the future development of theories in biological control. Handling Editor: Helen Roy     

Does cowbird parasitism increase predation risk to American redstart nests?

Brood parasitism and nest predation are major causes of reproductive failure for many bird species nesting in fragmented landscapes. While brood parasites and predators may act independently, they could also interact if brood parasites increase the likelihood that predators detect nests. In this study, we examined the interaction between cowbird parasitism and nest predation in a 10 year study on 466 American redstart Setophaga ruticilla nests in central Alberta, Canada. We used advanced nest survival models to examine the support for three mechanisms that might lead to a positive correlation between brood parasitism and nest predation: 1) the presence of a cowbird nestling might increase the detection of the nest by predators, 2) nests with lower cover are more likely to be detected by both cowbirds and predators, and 3) cowbirds and predators may co-occur in landscapes of similar structure. Twelve percent of nests were parasitized and those nests had a 16–19% higher rate of failure due to predators compared to unparasitized nests. Daily nest predation rates increased during the nestling stage for both groups, but more strongly for parasitized nests. Loud begging by the cowbird nestling and/or higher parental feeding rates for the cowbird may have increased nest detectability to predators. Brood parasitism and nest predation were also positively related to forest cover, indicating landscape level effects were influential. Most nest predators were forest species and we suspect cowbirds responded positively to forest cover because of the increased abundance of songbird hosts. Nest-site features had less of an impact on nest predation or brood parasitism, although nests with higher overhead cover were less susceptible to predators. Our study shows how multiple mechanisms, particularly the behavioral effects of the brood parasite nestling and landscape structure, can lead to a positive relationship between nest predation and brood parasitism.